Robotic, laparoscopic or open hemihepatectomy for giant liver haemangiomas over 10 cm in diameter

Haemangioma is the most common benign lesion of the liver, occurring in the general population with a prevalence that ranges from 0.4 to 7.3% based on autopsy findings [1, 2]. The majority of liver haemangiomas are asymptomatic and are often discovered incidentally during imaging investigations for various unrelated pathologies. Asymptomatic patients with liver haemangiomas less than 5 cm in diameter require observation and no intervention [3]. Surgical treatment for liver haemangioma is required in lesions larger than 5 cm in diameter, when there are symptoms or complications, or when the diagnosis is uncertain [4]. The main treatments for liver haemangioma include transarterial embolization (TAE), enucleation, liver resection, and transplantation. A giant liver haemangioma is defined as a liver haemangioma with a minimum size of 10 cm [5]. While some surgeons have reported that enucleation is safer and quicker than resection [6, 7], others have concluded that there is no significant difference between enucleation and resection [8, 9]. Mark S et al. [10] suggested that liver resection was preferable for lesions that completely occupied an anatomical section of the liver. Open liver resection requires a large abdominal incision and long recovery time. Increasing numbers of operations are now performed with minimally invasive surgery with either laparoscopic or robotic surgery [11]. To our knowledge, no study has been reported that has compared robotic, laparoscopic, and open liver resection for giant liver haemangiomas. The present study was undertaken to evaluate the clinical efficacy of robotic, laparoscopic and open hemihepatectomy for giant liver haemangioma.

During the study period, 326 patients underwent liver resection for liver haemangioma, and 128 patients had giant liver haemangiomas (defined as a liver haemangioma with a diameter > 10 cm). Hemihepatectomies were carried out in 57 of these patients with giant liver haemangiomas. RH was carried out in 19 patients, LH in 13 patients, and OH in 25 patients. There were no significant differences in age, sex, tumour location, BSA, FLR, SLV, liver haemangioma volume, FLR/SLV, resected normal liver volume/resected volume, or hepatic disease among the three groups (Table 1).

There were no significant differences in the rates of blood transfusion (P>0.05, Table 2) among the three groups. The operative time of the OH group was significantly shorter than that of the RH group and the LH group (190.2 ± 51.8 vs 256.3 ± 57.7 and 268.4 ± 93.6 min, P<0.05, Tables 2, 4), while there was no significant difference between the RH group and the LH group (P>0.05, Table 4). When the setup time in the RH group was excluded, the operative time of the RH group was significantly shorter than that of the LH group (216.3 ± 57.7 vs 268.4 ± 93.6 min, P<0.05, Tables 2, 4), while there was no significant difference between the RH group and the OH group (190.2 ± 51.8 vs 216.3 ± 57.7, P>0.05, Table 4). The amount of intraoperative blood loss in the RH group was significantly the lower among the three groups (319.5 ± 206.0 vs 476.9 ± 210.8 and 628.0 ± 231.0 ml, P<0.05, Tables 2, 4), and the amount of intraoperative blood loss in the LH group was significantly less than that in the OH group (476.9 ± 210.8 vs 628.0 ± 231.0 ml, P<0.05, Tables 2, 4). Compared with patients in the RH group and the LH group, patients in the OH group had a significantly longer postoperative hospital stay (7.2 ± 2.3 vs 5.5 ± 2.1 and 4.7 ± 1.7 d), time to oral intake (3.1 ± 1.1 vs 2.2 ± 1.1 and 1.9 ± 0.9 d), and time to get-out-of-bed (2.8 ± 0.9 vs 1.8 ± 0.7 and 1.7 ± 0.8 d) as well as a significantly higher VAS score after 24 h of surgery (4.9 ± 1.3 vs 2.5 ± 1.0 and 2.3 ± 0.9) (P < 0.05 each) (Tables 3, 4), while there were no significant differences in these variables between the RH group and the LH group (P>0.05, Table 4). There was no significant difference in liver function after 24 h of surgery among the three groups (P>0.05, Table 3). No postoperative deaths occurred in this study, and 3 patients (5.3%) developed complications, which included gastric retention (n = 1) and biliary leakage (n = 2) (Table 3). The data for the follow-up visits 3 months after the operations were available for all 57 patients. Four patients (7.0%) had persistent or recurrent preoperative symptoms: 2 patients with abdominal pain, 1 with nausea, and 1 with premature satiety after meals (Table 5).

Haemangioma is a common benign lesion of the liver. It originates from the mesodermal layer and represents a congenital, non-neoplastic hamartomatous proliferation of vascular endothelial cells [15]. Asymptomatic patients with liver haemangiomas less than 5 cm in diameter require only monitoring through imaging examinations every 6 months or annually to assess the progression of disease [3, 11]. The common indications for surgical treatment in symptomatic patients with liver haemangiomas larger than 5 cm in diameter are pain, rapid growth in size, uncertainty of malignancy, local compression, spontaneous or traumatic rupture, and Kasabach-Merritt syndrome [5, 10]. Since the first resection of liver haemangioma reported by Hermann Pfannenstiel in 1898, the treatments for liver haemangioma have included TAE, enucleation, liver resection, and transplantation [16, 17]. TAE can be used to reduce the size of giant liver haemangiomas and decrease the risk of bleeding during resection. However, vascular recanalization leading to recurrence is common [18‐20]. Symptomatic patients with unresectable lesions or multiple haemangiomas are indicated for liver transplantation [21]. Haemangioma is a well-circumscribed, hypervascular and compressible lesion with a clear sheath of compressed liver parenchyma between the haemangiomatous tissues and the normal liver [22]. Enucleation can be performed to remove the liver haemangioma with its surrounding fibrous capsule, which is composed of compressed liver parenchyma. Several authors have reported that enucleation of giant haemangiomas is safer and quicker than liver resection, with better preservation of the liver parenchyma, less morbidity, and less blood loss [6, 7]. On the other hand, Wang et al. [23] concluded that the operative time, blood loss, and blood transfusion requirements for anatomic liver resections were similar to those for enucleation. When a liver haemangioma is giant or when it is at a dangerous anatomical location adjacent to the inferior vena cava or a major hepatic vein, enucleation may cause massive intraoperative blood loss. In such patients, liver resection may be a better approach [24, 25]. In hepatic resection, the FLR volume, SLV and TLV have been used to predict postoperative hepatic dysfunction [26]. Although the safety limit of the FLV remains controversial, several studies have shown that an FLR/TLV ratio of ≤20% is associated with increased complications and a higher likelihood of postoperative hepatic dysfunction in noncirrhotic patients. In our study, the FLR/SLV ratio was between 33.2 and 41.2%, and the resected normal liver volume/resected volume was only between 14.2 and 17.4%. These ratios suggested that there were adequate remnant liver volumes and small losses of normal hepatic parenchyma in our patients. To balance the risk of massive intraoperative bleeding and the preservation of normal hepatic parenchyma, our team prefers to perform hemihepatectomy rather than enucleation for patients without cirrhosis and hepatitis whenever technically possible. To decrease excessive intraoperative blood loss in hemihepatectomy, our team routinely uses selective hemihepatic inflow occlusion for hemihepatectomy and the modified Pringle’s manoeuvre to occlude the inflow of the entire liver when necessary.

The traditional open approach requires a large abdominal incision, which is often associated with a long recovery time. Since the first truly laparoscopic anatomical liver resection in the form of a left lateral sectionectomy was reported in 1996 by Azagra et al., laparoscopic liver resection rapidly progressed and became popular [27]. The main advantages of minimally invasive liver resection over other techniques are its significantly shorter postoperative hospital stay and lower morbidity [28‐30]. Robotic surgery is a further development of the minimally invasive technique. The robotic system provides magnified three-dimensional imaging, tremor filtering and motion scaling. Endowrist technology with seven degrees of freedom allows smooth and precise movements that are required in liver resection [31].

The current study aimed to evaluate the clinical efficacy of robotic, laparoscopic, and open hemihepatectomy for giant liver haemangioma carried out by a single team of experienced liver surgeons. Robotic and laparoscopic hemihepatectomies were associated with the following advantages over open hemihepatectomy in our study: less intraoperative blood loss, a shorter postoperative hospital stay, an earlier time to get-out-of bed and earlier oral intake, and a lower VAS score after 24 h of surgery. The modified Pringle’s manoeuvre made the control of bleeding as easy in the RH group and the LH group as in the OH group. The minimal manipulation and the small incision were correlated with less bleeding, a faster postoperative recovery and better pain control. All physicians in our teams were skilled in performing open, robotic and laparoscopic hemihepatectomies. Due to limited two-dimensional vision in laparoscopic surgery, giant liver haemangiomas resulted in limited manipulating space in the LH group, a long setup time in robotic surgery, and a longer operative time in the LH and RH groups. If the setup time in the RH group was excluded, the operative time was significantly shorter in the RH group than in the LH group, while there was no significant difference between the RH and OH groups. The amount of intraoperative blood loss was significantly greater in the LH group than in the RH group. The precise movement and three-dimensional view of the operative field were probably the reasons for the lower amount of bleeding and shorter operation time in robotic hemihepatectomy than in laparoscopic hemihepatectomy. Our study also showed that no significant difference existed among the three groups in terms of the rates of blood transfusion and in the liver function after 24 h of surgery. Yu et al. [32] reported that the levels of ALT and AST after operations in the laparoscopic liver resection group were lower than those in the open liver resection group. Our study also showed no significant differences in postoperative hospital stay, time to oral intake, time to get-out-of bed or VAS scores between the RH and LH groups. Furthermore, most symptoms, such as abdominal pain and nausea, were relieved after hemihepatectomy.

The major limitations of this study are the small sample size and the short duration of follow-up, which may have generated bias in the interpretation of the results. Further multicentre randomized controlled clinical studies with larger sample sizes and longer follow-up periods are needed.

Robotic and laparoscopic hemihepatectomies were associated with less intraoperative blood loss, less postoperative pain, better postoperative recovery, and a shorter postoperative hospital stay. Compared with laparoscopic surgery, robotic hemihepatectomy was associated with significantly less intraoperative blood loss and a shorter operative time.